JOURNAL OF NATURAL HISTORY, 2016 http://dx.doi.org/10.1080/00222933.2016.1190416 Helminths of 13 species of microhylid frogs (Anura: Microhylidae) from Papua New Guinea Stephen R. Goldberga, Charles R. Burseyb and Fred Krausc aDepartment of Biology, Whittier College, Whittier, CA, USA; bDepartment of Biology, Pennsylvania State University, Shenango Campus, Sharon, PA, USA; cDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA ABSTRACT ARTICLE HISTORY In an attempt to better document the invertebrate biodiversity of the Received 8 December 2015 threatened fauna of Papua New Guinea (PNG), 208 microhylid frogs Accepted 27 April 2016 representing 13 species collected in 2009 and 2010 in PNG were KEYWORDS examined for endoparasitic helminths. This study found mature indi- Endoparasites; microhylid viduals of one species of Digenea (Opisthioglyphe cophixali), adults of frogs; Microhylidae; Papua two species of Cestoda (Nematotaenia hylae, Cylindrotaenia sp.) and New Guinea cysticerci of an unidentified cestode species; adults of nine species of Nematoda (Aplectana krausi, Bakeria bakeri, Cosmocerca novaeguineae, Cosmocercella phrynomantisi, Falcaustra papuensis, Icosiella papuensis, Ochtoterenella papuensis, Parathelandros allisoni, Parathelandros ander- soni), and one species of Acanthocephala (cystacanths in the family Centrorhynchidae). There was a high degree of endemism among the helminth species infecting the microhylids, with 83% of the species known only from PNG. Yet the helminth fauna infecting Papuan microhylidsaregeneralistswithdirect life cycles (no intermediate host) that also infect other anuran species. We thus conclude infection is more dependent upon habitat conditions than diet. Twenty-nine new host records are reported. Introduction The landscape of Papua New Guinea (PNG) is threatened with habitat loss due to logging and resultant forest loss, conversion of land for agriculture, mining, removal Downloaded by [University of Cambridge] at 00:03 21 June 2016 of oil and natural gas, and habitat modification and competition from invasive exotic species (Marshall and Beehler 2007a). In view of these threats to the environment, it is crucial to document both invertebrate and vertebrate diversity in Papuan fauna while it is possible. Frogs are particularly sensitive to environmental degradation and many species have suffered serious population declines (Lips and Donnelly 2005). With the above in mind, an examination of frogs for helminths will add to our knowledge of invertebrate biodiversity from a threatened area. Knowledge of tropical biodiversity is still very imperfect, and this is especially true for the invertebrates, which encompass the vast majority of species diversity. Helminths form a major portion of this diversity, and they can be important in CONTACT Stephen R. Goldberg [email protected] Department of Biology, Whittier College, Whittier, CA 90608, USA © 2016 Informa UK Limited, trading as Taylor & Francis Group 2 S. R. GOLDBERG ET AL. structuring vertebrate community structure (Poulin 2001), yet knowledge of tropical helminth communities is especially sparse (Choudhury and Dick 2000). Because frogs are particularly sensitive to environmental degradation (Pough et al. 2016), many species have suffered serious population declines (Lannoo 2005). Undoubtedly con- sequent with those declines but typically unstudied, it may be expected that the helminth faunas of those host frogs have also declined, in some cases perhaps to the point of extinction. The family Microhylidae occurs on all continents except Antarctica (Vitt and Caldwell 2014), and contains ca. 578 species, of which 287 occur in the Papuan region (= New Guinea, the Bismarck and Admirality archipelagos, and the Solomon Islands) and 192 occur in the country of PNG (Frost 2015). Approximately half of the frogs in New Guinea belong to the Microhylidae (Marshall and Beehler 2007b). In this paper, we present helminthological records for 13 species of microhylid frogs from PNG: Choerophryne darlingtoni (Loveridge, 1948); Choerophryne gudrunae (Menzies, 1999); Cophixalus balbus Günther, 2003; Cophixalus desticans Kraus and Allison, 2009; Cophixalus variabilis Kraus and Allison, 2006a; Cophixalus verrucosus (Boulenger 1898); Hylophorbus richardsi Günther, 2001; Oreophryne biroi (Méhely, 1897); Oreophryne geislerorum (Boettger, 1892); Oreophryne notata Zweifel, 2003; Oreophryne parkeri Loveridge, 1955; Sphenophryne cornuta Peters and Doria, 1878;andXenorhina oxyce- phala (Schlegel, 1858). Herein, the initial helminth lists are presented for eight frog species, and the helminth lists for another five species are expanded. Choerophryne darlingtoni is known from the central mountain ranges of PNG, being reported from Southern Highlands, Eastern Highlands, Chimbu and Western Highlands provinces (Menzies 2006; Kraus 2010). Choerophryne gudrunae is endemic to the Adelbert Mountains, Madang Province, PNG (Menzies 1999). Cophixalus balbus is known from several mountain ranges along the northern coast of New Guinea and from adjacent Yapen Island (Günther 2003; Kraus and Allison 2006b; Kraus unpubl. data). Cophixalus desticans is known from Milne Bay and Northern provinces, PNG (Kraus and Allison 2009; Kraus 2013). Cophixalus variabilis and C. verrucosus are known from Milne Bay, Central and Northern provinces, Papua New Guinea (Kraus and Allison 2006a; Kraus 2010; unpubl. data). Hylophorbus richardsi is known only from the vicinity of the type locality on Mount Sisa and the eastern slope of Mount Itukua, Muller Range, Southern Highlands Province, PNG (Günther 2001; Kraus 2010). Oreophryne biroi Downloaded by [University of Cambridge] at 00:03 21 June 2016 is known from the northern coastal region of New Guinea from the vicinity of Madang, Madang Province, PNG, to the Cyclops Mountains near Jayapura, Papua, Indonesia (Zweifel et al. 2003). Oreophryne geislerorum ranges from the Huon Peninsula, westward to Lae and the Wampit River and from there south through Northern Province, and into the north- ern end of Milne Bay Province, PNG (Zweifel et al. 2003; Kraus unpubl. data). Oreophyrne notata occurs in the Central Highlands area of PNG Southern Highlands Province west to near the border with Indonesia (Zweifel 2003). Oreophryne parkeri is known from the north-coast area of New Guinea (Zweifel et al. 2003). Sphenophryne cornuta is widely distributed in New Guinea from the Vogelkop Peninsula (Papua, Indonesia) to the vicinity of Port Moresby (PNG) and to the Adelbert Mountains, PNG (Menzies 2006)andXenorhina oxycephala is known from Western Papua (Indonesia) as well as the north-coast ranges of Papua (Indonesia) and PNG (Zweifel 1972). Areas JOURNAL OF NATURAL HISTORY 3 Figure 1. Map of New Guinea showing the four areas from which our samples were collected. Square = Muller Range, Southern Highlands Province; triangle = Prince Alexander Mts., East Sepik Province; circle = Adelbert Mts., Madang Province; diamond = Mt. Victory, Northern Province. in PNG where the frogs were collected are indicated in Figure 1. Geographic ranges for the above frog species can be found by searching under the species name at http://www.iucnredlist.org. Materials and methods Two hundred and eight adult frogs representing 13 species of Microhylidae were collected by hand in PNG (Figure 1) by Fred Kraus during 2009 and 2010 (collection dates for each species are indicated in Appendix 1) and were examined for endopar- asites: Choerophryne darlingtoni (n = 5), Choerophryne gudrunae (n = 19), Cophixalus balbus (n = 12), Cophixalus desticans (n = 19), Cophixalus variabilis (n = 36), Cophixalus verrucosus (n = 9), Hylophorbus richardsi (n = 13), Oreophryne biroi (n = 5), Oreophryne geislerorum (n = 29), Oreophryne notata (n = 35), Oreophryne parkeri (n = 6), Downloaded by [University of Cambridge] at 00:03 21 June 2016 Sphenophryne cornuta (n = 16) and Xenorhina oxycephala (n = 4). Immediately after capture, frogs were euthanised and fixed in neutral buffered 10% formalin, and were later stored in 70% ethanol in the herpetology collection of the Bishop Museum (BPBM), Honolulu, Hawaii (Appendix 1). Subsequently, the body cavity was opened by a longitudinal abdominal incision, and the gastrointestinal tract was removed by cutting across the esophagus and the rectum and then shipped to Whittier College, Whittier, CA, where a detailed dissection of each digestive organ was carried out using a dissecting microscope. Endoparasites from individual hosts were removed to vials of 70% ethanol, and later placed on a microscope slide in a drop of lactophenol under a coverslip and allowed to clear. Nematodes and acanthocephalans were identi- fied from these temporary preparations. Digeneans and cestodes were washed in water, regressively stained in hematoxylin, and mounted in balsam for identification under a compound microscope. Parasite terminology used herein is in accordance with Bush 4 S. R. GOLDBERG ET AL. et al. (1997). The number of parasites, prevalence, mean intensity, range of infection and new host records are given in Table 1. Hosts for helminths reported in Paupan frogs are summarised in Table 2. Selected helminth specimens were deposited in the Harold W. Manter Parasitology Laboratory (HWML), University of Nebraska, Lincoln, USA (Appendix 2). Results A total of 360 endoparasites was recovered from 88 (42%) of the 208 frogs (Table 1). Of these, 220 (61%) were mature individuals representing one species of Digenea: Opisthioglyphe cophixali Moravec and Sey,